Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction
Grégory Hoff,
Anthony Arguelles Arias,
Farah Boubsi,
Jelena Pršić,
Thibault Meyer,
Heba M. M. Ibrahim,
Sébastien Steels,
Patricio Luzuriaga,
Aurélien Legras,
Laurent Franzil,
Michelle Lequart-Pillon,
Catherine Rayon,
Victoria Osorio,
Edwin de Pauw,
Yannick Lara,
Estelle Deboever,
Barbara de Coninck,
Philippe Jacques,
Magali Deleu,
Emmanuel Petit,
Olivier Van Wuytswinkel,
Marc Ongena
Affiliations
Grégory Hoff
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Anthony Arguelles Arias
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Farah Boubsi
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Jelena Pršić
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Thibault Meyer
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Heba M. M. Ibrahim
Division of Plant Biotechnics, Department of Biosystems, Faculty of Bioscience Engineering, KU Leuven, Leuven, Belgium
Sébastien Steels
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Patricio Luzuriaga
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Aurélien Legras
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Laurent Franzil
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Michelle Lequart-Pillon
Unité Biologie des Plantes et Innovation, BioEcoAgro, Joint Research Unit/UMR Transfrontalière 1158, Université de Picardie Jules Verne, UFR des Sciences, Amiens, France
Catherine Rayon
Unité Biologie des Plantes et Innovation, BioEcoAgro, Joint Research Unit/UMR Transfrontalière 1158, Université de Picardie Jules Verne, UFR des Sciences, Amiens, France
Victoria Osorio
Mass Spectrometry Laboratory, MolSys Research Unit, Department of Chemistry, University of Liège, Liège, Belgium
Edwin de Pauw
Mass Spectrometry Laboratory, MolSys Research Unit, Department of Chemistry, University of Liège, Liège, Belgium
Yannick Lara
Astrobiology, UR-ASTROBIOLOGY, Geology Department, University of Liège, Liège, Belgium
Estelle Deboever
Molecular Biophysics at Interfaces Laboratory, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
Barbara de Coninck
Division of Plant Biotechnics, Department of Biosystems, Faculty of Bioscience Engineering, KU Leuven, Leuven, Belgium
Philippe Jacques
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
Magali Deleu
Molecular Biophysics at Interfaces Laboratory, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
Emmanuel Petit
Unité Biologie des Plantes et Innovation, BioEcoAgro, Joint Research Unit/UMR Transfrontalière 1158, Université de Picardie Jules Verne, UFR des Sciences, Amiens, France
Olivier Van Wuytswinkel
Unité Biologie des Plantes et Innovation, BioEcoAgro, Joint Research Unit/UMR Transfrontalière 1158, Université de Picardie Jules Verne, UFR des Sciences, Amiens, France
Marc Ongena
Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit/UMR transfrontalière 1158, University of Liège‐Gembloux Agro‐Bio Tech, Gembloux, Belgium
ABSTRACT Bacillus velezensis is considered as a model species belonging to the so-called Bacillus subtilis complex that evolved typically to dwell in the soil rhizosphere niche and establish an intimate association with plant roots. This bacterium provides protection to its natural host against diseases and represents one of the most promising biocontrol agents. However, the molecular basis of the cross talk that this bacterium establishes with its natural host has been poorly investigated. We show here that these plant-associated bacteria have evolved a polymer-sensing system to perceive their host and that, in response, they increase the production of the surfactin-type lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favored upon growth on root exudates and that this lipopeptide is a key component used by the bacterium to optimize biofilm formation, motility, and early root colonization. In this specific nutritional context, the bacterium also modulates qualitatively the pattern of surfactin homologues coproduced in planta and forms mainly variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. IMPORTANCE Within the plant-associated microbiome, some bacterial species are of particular interest due to the disease protective effect they provide via direct pathogen suppression and/or stimulation of host immunity. While these biocontrol mechanisms are quite well characterized, we still poorly understand the molecular basis of the cross talk these beneficial bacteria initiate with their host. Here, we show that the model species Bacillus velezensis stimulates the production of the surfactin lipopeptide upon sensing pectin as a cell surface molecular pattern and upon feeding on root exudates. Surfactin favors bacterial rhizosphere fitness on one hand and primes the plant immune system on the other hand. Our data therefore illustrate how both partners use this multifunctional compound as a unique shared good to sustain a mutualistic interaction.